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Multiple-Insecticide Resistance in Anopheles Gambiae Mosquitoes, Southern Côte D'ivoire

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Multiple-Insecticide Resistance in Anopheles Gambiae Mosquitoes, Southern Côte D'ivoire DISPATCHES example, in several populations of the major malaria vector Multiple-Insecticide in Africa, Anopheles gambiae s.l. mosquitoes, mutations in the DDT/pyrethroid target site, known as knockdown Resistance in resistance (kdr) alleles, have been found in conjunction with resistance alleles of the acetylcholinesterase Anopheles gambiae gene (Ace-1R), the target site of organophosphates and carbamates (5). To date, however, these cases of multiple- Mosquitoes, insecticide resistance have been restricted by the relatively Southern Côte low prevalence of organophosphate/carbamate resistance and the limited effect that kdr mutations alone have on d’Ivoire pyrethroid-based interventions (6). We report a population of An. gambiae mosquitoes from a rice-growing area of Constant V.A. Edi, Benjamin G. Koudou, southern Côte d’Ivoire that have high frequencies of kdr Christopher M. Jones, David Weetman, and Ace-1R alleles and unprecedentedly high levels of and Hilary Ranson phenotypic resistance to all insecticide classes available for Malaria control depends on mosquito susceptibility to malaria control. insecticides. We tested Anopheles gambiae mosquitoes from Côte d’Ivoire for resistance and screened a subset The Study for target site mutations. Mosquitoes were resistant to During May–September 2011, mosquito larvae were insecticides of all approved classes. Such complete collected in irrigated rice fi elds surrounding Tiassalé, resistance, which includes exceptionally strong phenotypes, southern Côte d’Ivoire (5°52′47′′N; 4°49′48′′W) and reared presents a major threat to malaria control. to adults in insectaries on a diet of MikroMin (Tetra, Melle, Germany) fi sh food. A total of 1,571 adult female An. argeting the mosquito vector is the most effective way to gambiae s.l. mosquitoes, 3–5 days of age, were exposed Tprevent malaria transmission; worldwide, this method to 1 of 5 insecticides (0.1% bendiocarb, 1.0% fenitrothion, accounts for more than half of malaria control expenditures 0.75% permethrin, 0.05% deltamethrin, 4% DDT) or a (1,2). During the past decade, increased use of insecticide- control paper for 1 hour, according to standard WHO treated bed nets and indoor residual spraying have made procedures (7). Mosquito deaths were recorded 24 hours a pivotal contribution toward decreasing the number of later. DNA was extracted from individual mosquitoes malaria cases (1). However, these gains are threatened by according to the LIVAK method (8), and a subsample of the rapid development and spread of insecticide resistance 500 mosquitoes were all found to be the M molecular form among major malaria vectors in Africa (3). To keep vector of An. gambiae s.s. by using the SINE-PCR method (9). R resistance from undermining control programs, insecticide- The target site mutation G119S in the Ace-1 gene (Ace-1 ) resistance management strategies must reduce the current and L1014F and L1014S kdr mutations were screened by overreliance on pyrethroids. These compounds are used using restriction fragment length polymorphism (10) or widely for indoor residual spraying and uniquely for TaqMan assays (11), respectively. insecticide-treated bed nets. However, having a limited According to WHO criteria, An. gambiae mosquitoes number of insecticides available for malaria vector from Tiassalé are resistant to all insecticide classes, control restricts options for effective insecticide resistance and resistance is extremely prevalent; more than two management. Only 4 classes of insecticide, which share thirds of mosquitoes survived the diagnostic dose for 2 modes of action, are approved by the World Health 4 of the 5 insecticides tested (Table 1). To assess the Organization (WHO). level of resistance, we exposed the Tiassalé population A mutation at a single target site can result in mosquito and a susceptible laboratory population of An. gambiae resistance to DDT and pyrethroids or to organophosphates (Kisumu) mosquitoes to the pyrethroid deltamethrin or and carbamates. Furthermore, mosquitoes can express Table 1. Prevalence of insecticide resistance in Anopheles multiple insecticide-resistance mechanisms (4). For gambiae mosquitoes, M form, from Tiassalé, Côte d’Ivoire, 2011 Insecticide No. tested* No. dead % Dead (95% CI) Author affi liations: Liverpool School of Tropical Medicine, Liverpool, Permethrin 288 69 24.0 (19.1–29.3) UK (C.V.A. Edi, B.G. Koudou, C.M. Jones, D. Weetman, H. Deltamethrin 282 90 31.9 (26.5–37.7) Ranson); Centre Suisse de Recherches Scientifi ques en Côte DDT 306 25 8.2 (5.4–11.8) Fenitrothion 296 219 74.0 (68.6–78.9) d’Ivoire, Abidjan, Côte d’Ivoire (C.V.A. Edi, B.G. Koudou); and Bendiocarb 299 37 12.4 (8.9–16.6) Université d’Abobo-Adjamé, Abidjan (B.G. Koudou) *Measured by death within 24 h, after 1h exposure to each insecticide. All mosquitoes were resistant according to World Health Organization DOI: http://dx.doi.org/10.3201/eid1809.120262 classification (<80% dead) (7). 1508 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 9, September 2012 Insecticide Resistance in An. gambiae Mosquitoes resistance, and the absence of 119S homozygotes might be attributable to the high fi tness cost of the Ace-1R allele in the absence of insecticide (14). Presence of the 1014F kdr allele alone does not confer the ability to survive diagnostic doses of pyrethroids; thus, alternative mechanisms must be responsible for the high-level pyrethroid resistance in this population. The selective pressures responsible for this intense multiple-insecticide resistance in Tiassalé mosquitoes are unclear. There is a high coverage of insecticide-treated bed nets, but this coverage does not differ from that in other parts of the continent, and indoor residual spraying has not been conducted in this region. Use of insecticides in agriculture has been linked to resistance in malaria vectors. This use is perhaps the most likely explanation in this Figure 1. Time-mortality curve for wild-caught Anopheles gambiae district of intense commercial production of rice, cocoa, mosquitoes from Tiassalé, southern Côte d’Ivoire, exposed to and coffee. deltamethrin (median time to death = 248 minutes). Logistic regression line was fi tted to time-response data by using SigmaPlot Whatever the cause, the implications of this resistance version 11.0 (www.sigmaplot.com). R2 = 0.96. Error bars indicate scenario for malaria control are severe. With no new classes SEM. of insecticides for malaria control anticipated until 2020 at the earliest (15), program managers have few options available when confronted with multiple-insecticide the carbamate bendiocarb for a range of exposure times resistance. Assessing the effect of pyrethroid resistance and assessed deaths 24 hours later (online Technical on the effi cacy of insecticide-treated bed nets is complex Appendix, wwwnc.cdc.gov/EID/pdfs/12-0262-Techapp. because of the poorly understood associations between net pdf). We found an unexpectedly strong resistance integrity, insecticide content, net usage, and net effi cacy. phenotype to the 2 insecticides (Figures 1, 2). For delta- Nevertheless, resistance levels, such as those reported here, methrin, 4 hours of exposure were required to kill 50% combined with continual selection pressure will inevitably lead to suboptimal mosquito control by use of insecticide- (median lethal time, [LT50]); in comparison, the LT50 for the susceptible Kisumu strain was <2 minutes (resistance treated bed nets and indoor residual spraying. If unchecked, ratio = 138) (online Technical Appendix). Similarly, the this resistance could spread rapidly and threaten the fragile gains that have been made in reducing malaria across Africa. LT50 for bendiocarb was nearly 5 hours for the Tiassalé strain yet <12 minutes for the susceptible strain (resistance ratio = 24) (online Technical Appendix). To investigate the causes of this resistance, we screened a subset of mosquitoes for the target site mutations, kdr 1014F and 1014S. Only the 1014F kdr mutation was detected, and this resistance allele was found at high frequency (83%). There was a signifi cant association between presence of the 1014F kdr allele and ability to survive exposure to DDT but not to either pyrethroid (Table 2). In contrast, the Ace-1R allele was strongly associated with survival after exposure to bendiocarb and fenitrothion (Table 2). Conclusions Pyrethroid resistance in An. gambiae mosquitoes was fi rst reported from Côte d’Ivoire in 1993 (12); carbamate resistance was detected in the 1990s (13). Nevertheless, ≈2 decades later, it is surprising and worrying to fi nd Figure 2. Time-mortality curve for wild-caught Anopheles gambiae complete resistance to all insecticides tested, particularly— mosquitoes from Tiassalé, southern Côte d’Ivoire, exposed to bendiocarb (median time to death = 286 minutes). Logistic for deltamethrin and bendiocarb—at such high levels. regression line was fi tted to time-response data by using SigmaPlot Resistance mechanisms seem to be varied. Ace-1R is version 11.0 (www.sigmaplot.com). R2 = 0.88. Error bars indicate strongly associated with organophosphate and carbamate SEM. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 18, No. 9, September 2012 1509 DISPATCHES Table 2. Association between genotype and mosquito survival after insecticide exposure* No. per genotype Frequency† Insecticide No. tested Status No. LL LF FF 1014F‡ Odds ratio§ p value DDT 73 Alive 48 2 7 39 88.5 4 0.02 Dead 25 2 10 13 72 Permethrin 88 Alive 44 1 12 31 84.1 1.23 0.82 Dead 44 3 12 29 79.5 Deltamethrin 89 Alive 45 1 12 32 84.4 0.82 0.86 Dead 44 2 9 33 85.2 GG GS SS 119S¶ Bendiocarb 86 Alive 49 0 49 0 50 100 0.40 u 10–12 Dead 37 25 12 0 16.2 Fenitrothion 100 Alive 50 0 50 0 50 1,176 0 Dead 50 48 2 0 2 *F and L represent mutant resistant alleles (phenylalanine) and wild-type alleles (leucine), respectively; S and G represent mutant resistant alleles (serine) and wild-type alleles (glycine), respectively.
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